Circadian Regulation Does Not Optimize Stomatal Behaviour

Abstract

The circadian clock is a molecular timer of metabolism that affects the diurnal pattern of stomatal conductance (gs), amongst other processes, in a broad array of plant species. The function of circadian gs regulation remains unknown and here, we test whether circadian regulation helps to optimize diurnal variations in stomatal conductance. We subjected bean (Phaseolus vulgaris) and cotton (Gossypium hirsutum) canopies to fixed, continuous environmental conditions of photosynthetically active radiation, temperature, and vapour pressure deficit (free-running conditions) over 48 h. We modelled gs variations in free-running conditions to test for two possible optimizations of stomatal behaviour under circadian regulation: (i) that stomata operate to maintain constant marginal water use efficiency; or (ii) that stomata maximize C net gain minus the costs or risks of hydraulic damage. We observed that both optimization models predicted gs poorly under free-running conditions, indicating that circadian regulation does not directly lead to stomatal optimization. We also demonstrate that failure to account for circadian variation in gs could potentially lead to biased parameter estimates during calibrations of stomatal models. More broadly, our results add to the emerging field of plant circadian ecology, where circadian controls may partially explain leaf-level patterns observed in the field.

We acknowledge funding from the Natural Science Foundation in China (31850410483), the talent proposals in Sichuan Province (2020JDRC0065), and from Southwest University of Science and Technology. This study benefited from the CNRS human and technical resources allocated to the ECOTRONS Research Infrastructures as well as from the state allocation ‘Investissement d’Avenir’ AnaEE-France ANR-11-INBS-0001, ExpeER Transnational Access program, Ramón y Cajal fellowships (RYC-2012-10970 to VRD), Cotton Research and Development Corporation (CSP-1501 to DTT), a grant from the Velux Foundation, Switzerland (Project No. 1119 to AG and VRD), and an internal grant from UWS-HIE to VRD. W.R.A. acknowledges funding from the David and Lucille Packard Foundation, National Science Foundation grants 1714972 and 1802880, and the USDA National Institute of Food and Agriculture, Agricultural and Food Research Initiative Competitive Programme, Ecosystem Services and Agro-ecosystem Management, grant No. 2018-67019-27850.